vestibИзвестия Национальной академии наук Беларуси. Серия биологических наукProceedings of the National Academy of Sciences of Belarus, Biological Series1029-89402524-230XThe Republican Unitary Enterprise Publishing House "Belaruskaya Navuka"10.29235/1029-8940-2020-65-2-153-162vestib-663Research ArticleСтатьиВлияние повышенной температуры на перенос электронов в хлоропластах ячменяInfluence of elevated temperature on electron flows in chloroplasts of barleyПшибыткоН. Л.PshybytkoN. L.

Пшибытко Наталья Ленгиновна – канд. биол. наук, вед. науч. сотрудник

пр. Независимости 4, 220030, г. Минск

Natallia L. Pshybytko – Ph. D. (Biol.), Leading researcher

4, Nezavisimosti Ave., 220030, Minsk

pshybytko@bsu.byБачищеТ. С.BachyshchaT. S.

Бачище Татьяна Сергеевна – мл. науч. сотрудник

ул. Академическая, 27, 220072, г. Минск

Tatsiana S. Bachyshcha – Junior researcher

27, Akademicheskaya Str., 220072, Minsk

tatsiana.bachyshcha@gmail.comКабашниковаЛ. Ф.KabashnikovaL. F.

Кабашникова Людмила Федоровна – член-корреспондент, д-р биол. наук, доцент, заведующий лабораторией

ул. Академическая, 27, 220072, г. Минск

Liudmila F. Kabashnikova – Corresponding Member, D. Sc. (Biol.), Assistant Professor, Head of the Laboratory

27, Akademicheskaya Str., 220072, Minsk

kabashnikova@mail.ruБелорусский государственный университетBelarusian State UniversityИнститут биофизики и клеточной инженерии Национальной академии наук БеларусиInstitute of Biophysics and Cell Engineering of the National Academy of Sciences of Belarus202016052020652153162Copyright © Пшибытко Н.Л., Бачище Т.С., Кабашникова Л.Ф., 20202020Пшибытко Н.Л., Бачище Т.С., Кабашникова Л.Ф.Pshybytko N.L., Bachyshcha T.S., Kabashnikova L.F.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://vestibio.belnauka.by/jour/article/view/663

С использованием метода РАМ-флуориметрии оценена эффективность функционирования переносчиков электронов в тилакоидных мембранах необработанных и подвергшихся тепловому воздействию 7-дневных проростков ячменя. Исследованы переходные состояния темнота–свет в хлоропластах после теплового воздействия. Выявлены термоиндуцированные изменения протекания линейного и циклического транспорта электронов в хлоропластах. Показана активация НАД(Ф)Н-зависимого электронного потока после воздействия повышенной температуры. Высказано предположение о регуляторной роли ΔрН тилакоидных мембран в распределении потоков электронов и адаптации фотосинтетического аппарата к стрессовым воздействиям.

The efficiency of electron carriers in thylakoid membranes untreated and exposed to heat 7-day-old barley seedlings was evaluated with PAM fluorescence. Darkness–light transitional states in chloroplasts after heat exposure are studied. Thermoinduced changes in linear and cyclic electron transport chain of chloroplasts are revealed. The activation of NADPH-dependent electron flux after exposure to elevated temperatures is shown. We assumed that ΔрН of thylakoid membranes employed the regulatory role in the distribution of electron flows and the adaptation of the photosynthetic apparatus to stressful effects.

фотосинтетический аппаратфотосистема 2электронные потоки в хлоропластахальтернативный транспорт электроновНАД(Ф)Н-оксидазатепловой шокРАМ-флуориметрияphotosynthetic apparatusphotosystem IIelectron flows in chloroplastsalternative electron transportNADPH-oxidaseheat shockРАМ-fluorescenceReferencesHe, M. Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance / M. He, Ch.-Q. He, N.-Zh. Ding // Frontiers Plant Sci. – 2018. – Vol. 9. – Art. 1771. https://doi.org/10.3389/fpls.2018.01771He M., He Ch.-Q., Ding N.-Zh. Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Frontiers in Plant Science, 2018, vol. 9, art. 1771. https://doi.org/10.3389/fpls.2018.01771Enhancing the abiotic stress tolerance of plants: from chemical treatment to biotechnological approaches / H.-Ch. Nguyen [et al.] // Physiologia Plantarum. – 2018. – Vol. 164, N 4. – P. 452–466. https://doi.org/10.1111/ppl.12812Nguyen H.-Ch., Lin K.-H., Ho Sh.-L., Chiang Ch.-M., Yang Ch.-M. Enhancing the abiotic stress tolerance of plants: from chemical treatment to biotechnological approaches. Physiologia Plantarum, 2018, vol. 164, no. 4, pp. 452–466. https://doi.org/10.1111/ppl.12812Plant responses and tolerance to high temperature stress: role of exogenous phytoprotectants / N. Kamrun [et al.] // Crop production and global environmental issues / ed. Kh. R. Hakeem. – Cham, 2015. – P. 385–435.Kamrun N., Hasanuzzaman M., Uddin Ahamed K., Rehman Hakeem Kh., Ozturk M., Fujita M. Plant responses and tolerance to high temperature stress: role of exogenous phytoprotectants. Crop production and global environmental issues. Cham, 2015, pp. 385–435.Carpentier, R. Effect of high-temperature stress on the photosynthetic apparatus / R. Carpentier // Books in soils, plants, and the environment / ed. M. Pessarakli. – New York, 1999. – P. 337–348.Carpentier R. Effect of high-temperature stress on the photosynthetic apparatus. Books in soils, plants, and the environment. New York, 1999, pp. 337–348.Derks, A. Diverse mechanisms for photoprotection in photosynthesis. Dinamic regulation of photosystem II excitation in response to rapin environmental change / A. Derks, K. Schaven, D. Bruce // Biochim. Biophys. Acta. Bioenergetics. – 2015. – Vol. 1847, N 4–5. – P. 468–485. https://doi.org/10.1016/j.bbabio.2015.02.008Derks A., Schaven K., Bruce D. Diverse mechanisms for photoprotection in photosynthesis. Dinamic regulation of photosystem II excitation in response to rapin environmental change. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 2015, vol. 1847, no. 4–5, pp. 468–485. https://doi.org/10.1016/j.bbabio.2015.02.008During state 1 to state 2 transition in arabidopsis thaliana, the photosystem II supercomplex gets phosphorylated but does not disassemble / E. Wientjes [et al.] // J. Biol. Chem. – 2013. – Vol. 288, N 46. – P. 32821–32826. https://doi.org/10.1074/jbc.m113.511691Wientjes E., Drop B., Kouřil R., Boekema E. J., Croce R. During state 1 to state 2 transition in arabidopsis thaliana, the Photosystem II supercomplex gets phosphorylated but does not disassemble. Journal of Biological Chemistry, 2013, vol. 288, no. 46, pp. 32821–32826. https://doi.org/10.1074/jbc.m113.511691Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo / G. Nagy [et al.] // Proc. Nat. Acad. Sci. – 2014. – Vol. 111, N 13. – P. 5042–5047. https://doi.org/10.1073/pnas.1322494111Nagy G., Ünnep R., Zsiros O., Tokutsu R., Takizawa K., Porcar L. [et al.]. Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. Proceedings of the National Academy of Sciences, 2014, vol. 111, no. 13, pp. 5042–5047. https://doi.org/10.1073/pnas.1322494111Nikkanen, L. Chloroplast thioredoxin systems dynamically regulate photosynthesis in plants / L. Nikkanen, E. Rintamäki // Biochem. J. – 2019. – Vol. 476, N 7. – P. 1159–1172. https://doi.org/10.1042/bcj20180707Nikkanen L., Rintamäki E. Chloroplast thioredoxin systems dynamically regulate photosynthesis in plants. Biochemical Journal, 2019, vol. 476, no. 7, pp. 1159–1172. https://doi.org/10.1042/bcj20180707Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants / T. Luo [et al.] // Plant Physiol. – 2012. – Vol. 159, N 1. – P. 118–130. https://doi.org/10.1104/pp.112.195446Luo T., Fan T., Liu Y., Rothbart M., Yu J., Zhou S., Grimm B., Luo M. Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants. Plant Physiology, 2012, vol. 159, no. 1, pp. 118–130. https://doi.org/10.1104/pp.112.195446Regulation of Rubisco activase and its interaction with Rubisco / A. R. Portis [et al.] // J. Exp. Bot. – 2007. – Vol. 59, N 7. – P. 1597–1604. https://doi.org/10.1093/jxb/erm240Portis A. R., Li C., Wang D., Salvucci M. E. Regulation of Rubisco activase and its interaction with Rubisco. Journal of Experimental Botany, 2007, vol. 59, no. 7, pp. 1597–1604. https://doi.org/10.1093/jxb/erm240Krause, G. H. Chlorophyll fluorescence and photosynthesis: the basics / G. H. Krause, E. Weis // Annu. Rev. Plant. Physiol. Mol. Biol. – 1991. – Vol. 42, N 1. – P. 313–349. https://doi.org/10.1146/annurev.arplant.42.1.313Krause G. H., Weis E. Chlorophyll fluorescence and photosynthesis: The basics. Annual Review of Plant Physiology and Plant Molecular Biology, 1991, vol. 42, no. 1, pp. 313–349. https://doi.org/10.1146/annurev.arplant.42.1.313Pfündel, E. Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system / E. Pfündel, Ch. Klughammer, U. Schreiber // PAM Application Notes. – 2008. – Vol. 1. – P. 21–24.Pfündel E., Klughammer Ch., Schreiber U. Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. PAM Application Notes, 2008, vol. 1, pp. 21–24.Robinson, H. H. Effect of manganese on the nuclear magnetic relaxivity of water protons in chloroplast suspensions / H. H. Robinson, R. R. Sharp, C. F. Yocum // Biochem. Biophys. Res. Commun. – 1980. – Vol. 93, N 3. – P. 755–761. https://doi.org/10.1016/0006-291x(80)91141-9Robinson H. H., Sharp R. R., Yocum C. F. Effect of manganese on the nuclear magnetic relaxivity of water protons in chloroplast suspensions. Biochemical and Biophysical Research Communications, 1980, vol. 93, no. 3, pp. 755–761. https://doi.org/10.1016/0006-291x(80)91141-9Гавриленко, В. Ф. Большой практикум по физиологии растений. Фотосинтез. Дыхание / В. Ф. Гавриленко, М. Е. Ладыгина, Л. М. Хандобина. – М. : Высш. шк., 1975. – 392 с.Gavrilenko V. F., Ladygina M. E., Khandobina L. M. Great workshop on plant physiology. Photosynthesis. Respiration. Moscow, Vysshaya shkola Publ., 1975. 392 p. (in Russian).Lowry, O. H. The determination of inorganic phosphate in the presence of labile phosphate esters / O. H. Lowry, J. A. Lopez // J. Biol. Chem. – 1946. – Vol. 162. – P. 421–428.Lowry O. H., Lopez J. A. The determination of inorganic phosphate in the presence of labile phosphate esters. Journal of Biological Chemistry, 1946, vol. 162, pp. 421–428.Pinton, R. Zinc deficiency enhanced NAD(P)H-dependent superoxide radical production in plasma membrane vesicles isolated from roots of bean plants / R. Pinton, I. Cakmak, H. Marschner // J. Exp. Bot. – 1994. – Vol. 45, N 1. – P. 45–50. https://doi.org/10.1093/jxb/45.1.45Pinton R., Cakmak I., Marschner H. Zinc deficiency enhanced NAD(P)H-dependent superoxide radical production in plasma membrane vesicles isolated from roots of bean plants. Journal of Experimental Botany, 1994, vol. 45, no. 1, pp. 45–50. https://doi.org/10.1093/jxb/45.1.45Protein measurement with the Folin phenol reagent / O. H. Lowry [et al.] // J. Biol. Chem. – 1951. – Vol. 193, N 1. – P. 265–275.Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 1951, vol. 193, no. 1, pp. 265–275.Карапетян, Н. В. Переменная флуоресценция хлорофилла как показатель физиологического состояния растений / Н. В. Карапетян, Н. Г. Бухов // Физиология растений. – 1986. – Т. 33, № 5. – С. 1013–1026.Karapetyan N. V., Bukhov N. G. Variable chlorophyll fluorescence as an indicator of the physiological state of plants. Fiziologiya rastenii [Plant physiology], 1986, vol. 33, no. 5, pp. 1013–1026 (in Russian).A four state parametric model for the kinetics of the non-photochemical quenching in Photosystem II / J. J. Snellenburg [et al.] // Biochem. Biophys. Acta. Bioenergetics. – 2017. – Vol. 1858, N 10. – P. 854–864. https://doi.org/10.1016/j.bbabio.2017.08.004Snellenburga J. J., Johnson M. P., Ruban A. V., van Grondelle R., van Stokkum I. H. M. A four state parametric model for the kinetics of the non-photochemical quenching in Photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 2017, vol. 1858, no. 10, pp. 854–864. https://doi.org/10.1016/j.bbabio.2017.08.004pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas / L. Tian [et al.] // Proc. Nat. Acad. Sci. – 2019. – Vol. 116, N 17. – P. 8320–8325. https://doi.org/10.1073/pnas.1817796116Tian L., Nawrocki W. J., Liu X., Polukhina I., van Stokkum I. H. M., Croce R. pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas. Proceedings of the National Academy of Sciences, 2019, vol. 116, no. 17, pp. 8320–8325. https://doi.org/10.1073/pnas.1817796116Ruban, A. V. The photoprotective molecular switch in the photosystem II antenna / A. V. Ruban, M. P. Johnson, Ch. D. P. Duffy // Biochem. Biophys. Acta. – 2012. – Vol. 1817, N 1. – P. 167–181. https://doi.org/10.1016/j.bbabio.2011.04.007Ruban A. V., Johnson M. P., Duffy Ch. D. P. The photoprotective molecular switch in the photosystem II antenna. Biochimica et Biophysica Acta, 2012, vol. 1817, no. 1, pp. 167–181. https://doi.org/10.1016/j.bbabio.2011.04.007Miyake, Ch. Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions / Ch. Miyake // Plant Cell Physiol. – 2010. – Vol. 51, N 12. – P. 1951–1963. https://doi.org/10.1093/pcp/pcq173Miyake Ch. Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant and Cell Physiology, 2010, vol. 51, no. 12, pp. 1951–1963. https://doi.org/10.1093/pcp/pcq173Bukhov, N. Alternative photosystem I-driven electron transport routes: mechanisms and functions / N. Bukhov, R. Carpentier // Photosynth. Res. – 2004. – Vol. 82, N 1. – P. 17–33. https://doi.org/10.1023/b:pres.0000040442.59311.72Bukhov N., Carpentier R. Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynthesis Research, 2004, vol. 82, no. 1, pp. 17–33. https://doi.org/10.1023/b:pres.0000040442.59311.72Mulo, P. Chloroplast-targeted ferredoxin-NADP+ oxidoreductase: structure, function and location / P. Mulo // Biochem. Biophys. Acta. Bioenergetics. – 2011. – Vol. 1807, N 8. – P. 927–934. https://doi.org/10.1016/j.bbabio.2010.10.001Mulo P. Chloroplast-targeted ferredoxin-NADP+ oxidoreductase: structure, function and location. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 2011, vol. 1807, no. 8, pp. 927–934. https://doi.org/10.1016/j.bbabio.2010.10.001Cold stress effect on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications / L. V. Savitch [et al.] // Plant Cell Physiol. – 2011. – Vol. 52, N 6. – P. 1042–1054. https://doi.org/10.1093/pcp/pcr056Savitch L. V., Ivanov A. G., Gudynaite-Savitch L., Huner N. P. A. Simmonds J. Cold stress effect on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications. Plant and Cell Physiology, 2011, vol. 52, no. 6, pp. 1042–1054. https://doi.org/10.1093/pcp/pcr056Abolition of photosystem I cyclic electron flow in Arabidopsis thaliana following thermal-stress / J. Essemine [et al.] // Plant Physiol Biochem. – 2011. – Vol. 49, N 3. – P. 235–243. https://doi.org/10.1016/j.plaphy.2010.11.002Essemine J., Govindachary S., Ammar S., Bouzid S., Carpentier R. Abolition of photosystem I cyclic electron flow in Arabidopsis thaliana following thermal-stress. Plant Physiology and Biochemistry, 2011, vol. 49, no. 3, pp. 235–243. https://doi.org/10.1016/j.plaphy.2010.11.002Function of plastoquinone in heat stress reactions of plants / N. Pshybytko [et al.] // Biochim. Biophys. Acta. Bioenergetics. – 2008. – Vol. 1777, N 11. – P. 1393–1399. https://doi.org/10.1016/j.bbabio.2008.08.005Pshybytko N., Kruk J., Kabashnikova L., Strzalka K. Function of plastoquinone in heat stress reactions of plants. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 2008, vol. 1777, no. 11, pp. 1393–1399. https://doi.org/10.1016/j.bbabio. 2008.08.005Cyclic electron flow around photosystem I is essential for photosynthesis / Y. Munekage [et al.] // Nature. – 2004. – Vol. 429, N 6991. – P. 579–582. https://doi.org/10.1038/nature02598Munekage Y., Hashimoto M., Miyake C., Tomizawa K.-I., Endo T., Tasaka M., Shikanai T. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 2004, vol. 429, no. 6991, pp. 579–582. https://doi.org/10.1038/nature02598Joly, D. Regulation of energy dissipation in photosystem I by the redox state of the plastoquinone pool / D. Joly, R. Carpentier // Biochemistry. – 2007. – Vol. 46, N 18. – P. 5534–5541. https://doi.org/10.1021/bi602627dJoly D., Carpentier R. Regulation of energy dissipation in photosystem I by the redox state of the plastoquinone pool. Biochemistry, 2007, vol. 46, no. 18, pp. 5534–5541. https://doi.org/10.1021/bi602627dJoliot, P. Cyclic electron transfer in plant leaf / P. Joliot, A. Joliot // Proc. Nat. Acad. Sci. – 2002. – Vol. 99, N 15. – P. 10209–10214. https://doi.org/10.1073/pnas.102306999Joliot P., Joliot A. Cyclic electron transfer in plant leaf. Proceedings of the National Academy of Sciences, 2002, vol. 99, no. 15, pp. 10209–10214. https://doi.org/10.1073/pnas.102306999

The authors declare that there are no conflicts of interest present.